Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex

Abstract

AO_SCPLOWBSTRACTC_SCPLOWMotor (M1) and somatosensory (S1) cortex play a critical role in motor control but the nature of the signaling between these structures is not known. To fill this gap, we recorded - in three human participants whose hands were paralyzed as a result of a spinal cord injury - the responses evoked in the hand and arm representations of primary motor cortex (M1) while we delivered ICMS to the somatosensory cortex (S1). We found that ICMS of S1 activated some M1 neurons at short, fixed latencies, locked to each pulse in a manner consistent with monosynaptic activation. However, most of the changes in M1 firing rates were much more variable in time, suggesting a more indirect effect of the stimulation. The spatial pattern of M1 activation varied systematically depending on the stimulating electrode: S1 electrodes that elicited percepts at a given hand location tended to activate M1 neurons with movement fields at the same location. However, the indirect effects of S1 ICMS on M1 were strongly context dependent, such that the magnitude and even sign relative to baseline varied across tasks. We tested the implications of these effects for brain-control of a virtual hand, in which ICMS was used to convey tactile feedback about object interactions. While ICMS-evoked activation of M1 disrupted decoder performance, this disruption could be minimized with biomimetic stimulation, which emphasizes contact transients at the onset and offset of grasp, reduces sustained stimulation, and has been shown to convey useful contact-related information. SO_SCPLOWIGNIFICANCEC_SCPLOWMotor (M1) and somatosensory (S1) cortex play a critical role in motor control but the nature of the signaling between these structures is not known. To fill this gap, we recorded from M1 while delivering intracortical microstimulation (ICMS) to S1 of three human participants, whose hands were paralyzed by spinal cord injury. We found that ICMS activates M1 and that the motor fields of activated M1 neurons match the sensory fields of the stimulated S1 electrodes. These findings have important implications for using ICMS to convey tactile feedback for brain-controlled bionic hands. Indeed, the ICMS-evoked M1 activity worsens control of the hand. Fortunately, this effect is minimized by using biomimetic tactile feedback, which emphasizes contact transients and reduces sustained ICMS.